It has been known for several decades that rodents of a variety of species produce vocalizations during copulation, mother-pup interactions and other "social situations". In rats and mice, the species emphasized in this paper, the vocalizations usually consist of a single frequency band. When the frequency band is lowered electronically to a humanly audible level, the calls resemble brief whistles. These vocalizations have often been shown to play a role in regulating concomitant reproductive and maternal behavior.

In this paper we review what is known about ultrasonic communication in the most studied rodent species: house mice (Mus musculus), Norway rats (Rattus norvegicus). Work on Golden hamsters (Mesocricetus auratus) and other species is also briefly reviewed.

Copulation in House Mice

Spectral Characteristics of Mouse Calls

Two different ultrasonic calls have been identified in mice. One is a pure tone with a mean frequency of around 70 kHz and a duration of from 50 to 300 msec (Sales and Pye, 1974). The second is a pure tone around 40 kHz with a duration of 10 to just over 100 msec.

When Do the Vocalizations Occur?

Ultrasonic calls occur almost exclusively during reproduction. Moreover, by observing dyads of male/male, female/female and male/female pairs, Whitney, Coble, Stockton and Tilson (1973) provided evidence that the 70 kHz vocalizations are produced mainly by the male in this circumstance. More recent evidence involving surgical devocalization has confirmed this finding and extended it to 40 kHz vocalizations as well (White, Prasad, Barfield and Nyby, 1998).

When a male and female are placed together, the male emits 70 kHz vocalizations almost continuously prior to first mount during which time he actively sniffs and investigates the female. After the first mount, the amount of vocalizations declines, although during the latter stages of copulatory behavior, the male intermixes both 70 and 40 kHz calls immediately before and during each mounting bout (Nyby, 1983; Sales and Pye, 1974; White et al, 1998).

Female mice sometimes emit substantial amounts of vocalizations in response to other females (Maggio and Whitney, 1985) but whether these vocalizations have functional significance or are simply inappropriate male-typical behavior is not clear.

Stimuli That Elicit Ultrasonic Vocalizations from Male Mice.

Male mice emit ultrasonic vocalizations not only to a female mouse but also to any chemosignal that signals the presence of a female (Nyby, Wysocki Whitney and Dizinno, 1977). Female urine , female vaginal secretions, female saliva, and even previously neutral cues that are reliably paired with a female, all elicit male vocalizations (Nyby, Whitney, Schmitz and Dizinno, 1978; Nyby et al, 1979, Nyby, Whitney, Dizinno, Schneider and Nunez, 1981; Byatt and Nyby, 1986). More recent work has demonstrated the existence of a powerful but ephemeral ultrasound-eliciting pheromone in female urine that degrades via oxidation within 15-18 hours (Sipos and Nyby, 1992; Sipos, Nyby and Serran, 1993; Sipos, Alterman, Perry, Nyby and Vandenbergh, 1995 ). Adult males innately vocalize to this pheromone although responsiveness can be further enhanced by sexual experience in adulthood. Although males will also vocalize to a much longer lasting pheromone in aged urine (over 24 hours old), responsiveness to this latter signal requires adult sexual experience and the male rapidly habituates to this chemosignal alone. Although the urinary chemosignals that elicit ultrasounds are not present in female urine until after puberty, these chemosignals are nonetheless ovarian independent and, following puberty, are present in the urine at all stages of the female's estrous cycle (Nyby et al 1979).

How Does the Male Detect the Female Signals which Elicit Vocalizations?

Although chemosignals that elicit vocalizations can be detected by either the vomeronasal system or the primary olfactory system, the vomeronasal system appears to play a more central role (Wysocki, Nyby, Whitney, Beauchamp, and Katz, 1982 ). For example, males who have had the vomeronasal system removed prior to having had sexual experience during adulthood are relatively unresponsive olfactorially to chemosignals that normally elicit
ultrasounds. Denervation of the olfactory system prior to sexual experience, on the other hand, has little effect on vomeronasal responsiveness (Sipos, Wysocki, Nyby, Wysocki, and Nemura, 1995).

How Do Mouse Vocalizations Affect Reproductive Behavior?

Vocalizations by male mice have been hypothesized to serve a number of different functions. The vocalizations may signal the presence of a dominant male and deter subordinates (Nyby, Dizinno and Whitney, 1976), attract females from a distance (Nunez, Pomerantz, Bean and Youngstrom, 1985) reduce female aggression and withdrawal following courtship (Whitney and Nyby, 1979) and help coordinate copulatory behavior (White et al, 1998). However, definitive explanations await future research.

Endocrine Regulation of Vocalization in Mice

Male mouse vocalizations are androgen dependent. Vocalization amounts are reduced by castration and restored by androgen replacement (Nyby, Dizinno and Whitney 1976; Dizinno and Whitney, 1977). Androgen appears to act following aromatization to estradiol although the 5 alpha reduction pathway of testosterone action may be operative in some strains (Nyby and Simon, 1987). As with other male-typical behaviors, the best site for intracranial androgenic restoration is the medial preoptic area (Nyby, Matochik and Barfield, 1992; Matochik, Sipos, Nyby and Barfield, 1994 ). Virtually complete restoration of behavior to castrates is seen with implants in this area although some restoration is seen in other hypothalamic areas as well (Nyby et al, 1992).